Use of chemical tracers to assess diet and persistent organic pollutants in Antarctic Type C killer whales

Marine Mammal Science

Volumn 24, Issue 3, 2008, Pages 643-663

  Krahn, Margaret M ^a   Pitman, Robert L ^b   Burrows, Douglas G ^a   Herman, David P ^a   Pearce, Ronald W ^a  

^a NORTHWEST FISHERIES SCIENCE CENTER   (United States)

^b SOUTHWEST FISHERIES SCIENCE CENTER   (United States)

Author keywords

Antarctica; Biopsy sampling; Diet; Fatty acids; Killer whale; Orcinus orca; Persistent organic pollutants; Prey; Stable isotopes

Indexed keywords

ASSESSMENT METHOD; BIOASSAY; CONCENTRATION (COMPOSITION); DIET; ORGANIC POLLUTANT; PERSISTENCE; POLLUTION EXPOSURE; STATISTICAL ANALYSIS; TRACER; WHALE;

ANTARCTICA; PACIFIC OCEAN; PACIFIC OCEAN (TROPICAL);

CETACEA; MAMMALIA; ORCINUS ORCA; SPHENISCIDAE;

EID: 47749146167     PISSN: 08240469     EISSN: 17487692     Source Type: Journal    
DOI: 10.1111/j.1748-7692.2008.00213.x     Document Type: Article

References (74)

1. Ainley, D. G., G. Ballard and K. M. Dugger. 2006. Competition among penguins and cetaceans reveals trophic cascades in the western Ross Sea. Antarctica Ecology 87 : 2080 2093.
2. Aono, S., S. Tanabe, Y. Fujise, H. Kato and R. Tatsukawa. 1997. Persistent organochlorines in minke whale (Balaenoptera acutorostrata) and their prey species from the Antarctic and the North Pacific. Environmental Pollution 98 : 81 89.
3. Baird, R. W., P. A. Abrams and L. M. Dill. 1992. Possible indirect interactions between transient and resident killer whales: Implications for the evolution of foraging specializations in the genus Orcinus. Oecologia (Berlin) 89 : 125 132.
4. Ballard, G., and D. G. Ainley. 2005. Killer whale harassment of Adélie Penguins at Ross Island. Antarctic Science 17 : 385 386.
5. Barrett-Lennard, L. G. 2000. Population structure and mating patterns of killer whales as revealed by DNA analysis. Ph.D. thesis, University of British Columbia, Vancouver, BC. 108 pp.
6. Barrett-Lennard, L. G., J. K. B. Ford and K. A. Heise. 1996. The mixed blessing of echolocation: Differences in sonar use by fish-eating and mammal-eating killer whales. Animal Behaviour 51 : 553 565.
7. Berzin, A. A., and V. L. Vladimirov. 1983. A new species of killer whale (Cetacea, Delphinidae) from the Antarctic waters. Zoologichesky Zhurnal 62 : 287 295 In Russian).
8. Bigg, M. A. 1982. An assessment of killer whale (Orcinus orca) stocks off Vancouver Island, British Columbia. Report of the International Whaling Commission 32 : 655 666.
9. Borga, K., A. T. Fisk, P. F. Hoekstra and D. C. G. Muir. 2004. Biological and chemical factors of importance in the bioaccumulation and trophic transfer of persistent organochlorine contaminants in arctic marine food webs. Environmental Toxicology and Chemistry 23 : 2367 2385.
10. Burns, J. M., S. J. Trumble, M. A. Castellini and J. W. Testa. 1998. The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biology 19 : 272 282.
11. Cabana, G., and J. B. Rasmussen. 1996. Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Sciences of the United States of America 93 : 10844 10847.
12. Cherel, Y., and K. A. Hobson. 2007. Geographical variation in carbon stable isotope signatures of marine predators: A tool to investigate their foraging areas in the Southern Ocean. Marine Ecology-Progress Series 329 : 281 287.
13. Collins, M. 2006. Toothfish. Pages 1002 1004 in B. Riffenburgh, ed. Encyclopedia of the Antarctic. Routledge, New York, NY.
14. Connell, D. W., G. J. Miller, M. R. Mortimer, G. R. Shaw and S. M. Anderson. 1999. Persistent lipophilic contaminants and other chemical residues in the Southern Hemisphere. Critical Reviews in Environmental Science and Technology 29 : 47 82.
15. Coplen, T. B., W. A. Brand, M. Gehre, M. Gröning, H. A. J. Meijer, B. Toman and R. M. Verkouteren. 2006. New guidelines for d13C measurements. Analytical Chemistry 78 : 2439 2441.
16. Dahl, T. M., L. C., K. M. Kovacs, S. Falk-peterson, J. Sargent, I. Gjertz and G. B. Gulliksen. 2000. Fatty acid composition of the blubber in white whales (Delphinapterus leucas). Polar Biology 23 : 401 409.
17. DeNiro, M. J., and S. Epstein. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42 : 495 506.
18. DeNiro, M. J., and S. Epstein. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45 : 341 351.
19. DeWitt, H. H. 1970. The character of the midwater fish fauna of the Ross Sea, Antarctica. Pages 305 314 in M. W. Holdgate, ed. Antarctic Ecology. Academic Press, London, UK.
20. 13C measurements of Antarctic Peninsula fauna: Trophic relationships and assimilation of benthic seaweeds. American Zoologist 41 : 99 112.
21. Fisk, A. T., K. A. Hobson and R. J. Norstrom. 2001. Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the Northwater Polynya marine food web. Environmental Science & Technology 35 : 732 738.
22. Ford, J. K. B., and G. M. Ellis. 2006. Selective foraging by fish-eating killer whales Orcinus orca in British Columbia. Marine Ecology Progress Series 316 : 185 199.
23. Ford, J. K. B., G. M. Ellis, L. G. Barrett-Lennard, A. B. Morton, R. S. Palm and K. C. Balcomb. 1998. Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Canadian Journal of Zoology 76 : 1456 1471.
24. Ford, J. K. B., G. M. Ellis and K. C. Balcomb. 2000. Killer whales: The natural history and genealogy of Orcinus orca in British Columbia and Washington State. 2nd edition. UBC Press, Vancouver, BC, Canada.
25. Forney, K. A., and P. R. Wade. 2006. Worldwide distribution and abundance of killer whales. Pages 145 162 in J. A. Estes, D. P. Demaster, D. F. Doak, T. M. Williams and R. L. Brownell Jr., eds. Whales, whaling, and ocean ecosystems. University of California Press, Berkeley, CA.
26. Fox-Dobbs, K., J. K. Bump, R. O. Peterson, D. L. Fox and P. L. Koch. 2007. Carnivore-specific stable isotope variables and variation in the foraging ecology of modern and ancient wolf populations: Case studies from Isle Royale, Minnesota, and La Brea. Canadian Journal of Zoology 85 : 458 471.
27. Geochemical And Environmental Research Group. 2003. Spatial and temporal scales of human disturbance: McMurdo Station, Antarctica. Texas A&M University and University of Texas, Austin, College Station and Austin, TX.
28. Gill, P. C., and D. Thiele. 1997. A winter sighting of killer whales (Orcinus orca) in Antarctic sea ice. Polar Biology 17 : 401 404.
29. 2 in the world ocean. Global Biogeochemical Cycles 8 : 85 90.
30. Goerke, H., K. Weber, H. Bornemann, S. Ramdohr and J. Plotz. 2004. Increasing levels and biomagnification of persistent organic pollutants (POPs) in Antarctic biota. Marine Pollution Bulletin 48 : 295 302.
31. Hall-Aspland, S. A., T. L. Rogers and R. B. Canfield. 2005. Stable carbon and nitrogen isotope analysis reveals seasonal variation in the diet of leopard seals. Marine Ecology Progress Series 305 : 249 259.
32. Herman, D. P., D. G. Burrows, P. R. Wade, J. W. Durban, R. G. Leduc, C. O. Matkin and M. M. Krahn. 2005. Feeding ecology of eastern North Pacific killer whales from fatty acid, stable isotope, and organochlorine analyses of blubber biopsies. Marine Ecology Progress Series 302 : 275 291.
33. 15N analysis. Marine Ecology Progress Series 84 : 9 18.
34. Hobson, K. A., D. M. Schell, D. Renouf and E. Noseworthy. 1996. Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: Implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences 53 : 528 533.
35. 15N) model for the North Water food web: Implications for evaluating trophodynamics and the flow of energy and contaminants. Deep Sea Research Part II 49 : 5131 5150.
36. 13C) analyses. Marine Ecology Progress Series 198 : 273 281.
37. Hoekstra, P. F., T. M. O'Hara, A. T. Fisk, K. Borga, K. R. Solomon and D. C. G. Muir. 2003. Trophic transfer of persistent orgranochlorine contaminants (OCs) within an Arctic marine food web from the southern Beaufort-Chukchi Seas. Environmental Pollution 124 : 509 522.
38. Hoelzel, A. R., M. Dahlheim and S. J. Stern. 1998. Low genetic variation among killer whales (Orcinus orca) in the eastern north Pacific and genetic differentiation between foraging specialists. Journal of Heredity 89 : 121 128.
39. Hooker, S. K., S. J. Iverson, P. Ostrom and S. C. Smith. 2001. Diet of northern bottlenose whales inferred from fatty-acid and stable-isotope analyses of biopsy samples. Canadian Journal of Zoology 79 : 1442 1454.
40. Iverson, S. J., C. Field, W. D. Bowen and W. Blanchard. 2004. Quantitative fatty acid signature analysis: A new method of estimating predator diets. Ecological Monographs 74 : 211 235.
41. Jehl, J. R., Jr., W. E. Evans, F. T. Awbrey and W. S. Drieschmann. 1980. Distribution and geographic variation in the killer whale (Orcinus orca) populations of the Antarctic and adjacent waters. Antarctic Journal of the United States 15 : 161 163.
42. Jones, I. M. 2006. A northeast Pacific offshore killer whale (Orcinus orca) feeding on a Pacific halibut (Hippoglossus stenolepis). Marine Mammal Science 22 : 198 200.
43. Kelly, J. F. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78 : 1 27.
44. Kline, T. C., Jr. 1999. Temporal and spatial variability of 13C/12C and 15N/14N in pelagic biota of Prince William Sound. Canadian Journal of Fisheries and Aquatic Sciences 56 : 94 117.
45. Koopman, H. N., S. J. Iverson and D. E. Gaskin. 1996. Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena). Journal of Comparative Physiology. Part B 165 : 628 639.
46. Krahn, M. M., D. G. Burrows, J. E. Stein, P. R. Becker, M. M. Schantz, D. C. Muir and T. M. O'Hara. 1999. White whales (Delphinapterus leucas) from three Alaskan stocks: Concentrations and patterns of persistent organochlorine contaminants in blubber. Journal of Cetacean Research and Management 1 : 239 249.
47. Krahn, M. M., D. P. Herman, G. M. Ylitalo, C. A. Sloan, D. G. Burrows, R. C. Hobbs, B. A. Mahoney, G. K. Yanagida, J. Calambokidis and S. E. Moore. 2004. Stratification of lipids, fatty acids and organochlorine contaminants in blubber of white whales and killer whales. Journal of Cetacean Research and Management 6 : 175 189.
48. Krahn, M. M., D. P. Herman, C. O. Matkin, J. W. Durban, L. Barrett-Lennard, D. G. Burrows, M. E. Dahlheim, N. Black, R. G. Leduc and P. R. Wade. 2007. Use of chemical tracers in assessing the diet and foraging regions of eastern North Pacific killer whales. Marine Environmental Research 63 : 91 114.
49. La Mesa, M., J. T. Eastman and M. Vacchi. 2004. The role of notothenioid fish in the food web of the Ross Sea shelf waters: A review. Polar Biology 27 : 321 338.
50. Lauriano, G., C. M. Fortuna and M. Vacchi. 2007. Observation of killer whale (Orcinus orca) possibly eating penguins in Terra Nova Bay, Antarctica. Antarctic Science 19 : 95 96.
51. Mikhalev, Y. A., M. V. Ivashin, V. P. Savusin and F. E. Zelanaya. 1981. The distribution and biology of killer whales in the Southern Hemisphere. Report of the International Whaling Commission 31 : 551 566.
52. Muir, D. C. G., C. A. Ford, B. Rosenberg, R. J. Norstrom, M. Simon and P. Beland. 1996. Persistent organochlorines in beluga whales (Delphinapterus leucas) from the St. Lawrence River Estuary - I. Concentrations and patterns of specific PCBs, chlorinated pesticides and polychlorinated dibenzo-p-dioxins and dibenzofurans. Environmental Pollution 93 : 219 234.
53. Muir, D. C. G., P. D. Jones, H. Karlsson, K. Koczansky, G. A. Stern, K. Kannan, J. P. Ludwig, H. Reid, C. J. R. Robertson and J. P. Giesy. 2002. Toxaphene and other persistent organochlorine pesticides in three species of albatrosses from the North and South Pacific Ocean. Environmental Toxicology and Chemistry 21 : 413 423.
54. Olsen, E., and O. Grahl-Nielsen. 2003. Blubber fatty acids of minke whales: Stratification, population identification and relation to diet. Marine Biology 142 : 13 24.
55. Pitman, R. L., and P. Ensor. 2003. Three forms of killer whales (Orcinus orca) in Antarctic waters. Journal of Cetacean Research and Management 5 : 131 139.
56. Pitman, R. L., W. L. Perryman, D. Leroi and E. Eilers. 2007. A dwarf form of killer whale in Antarctica. Journal of Mammalogy 88 : 43 48.
57. Risebrough, R. W., B. W. Delappe and C. Younghans-Haug. 1990. PCB and PCT contamination in Winter Quarters Bay, Antarctica. Marine Pollution Bulletin 21 : 523 529.
58. Ross, P. S., G. M. Ellis, M. G. Ikonomou, L. G. Barrett-lennard and R. F. Addison. 2000. High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: Effects of age, sex and dietary preference. Marine Pollution Bulletin 40 : 504 515.
59. Sackett, W. M., W. R. Eckelmann, M. L. Bender and A. W. H. Be. 1965. Temperature dependence of carbon isotope composition in marine plankton and sediments. Science 148 : 235 237.
60. Schell, D. M., B. A. Barnett and K. A. Vinette. 1998. Carbon and nitrogen isotope ratios in zooplankton of the Bering, Chukchi and Beaufort seas. Marine Ecology Progress Series 162 : 11 23.
61. Sloan, C. A., D. W. Brown, R. W. Pearce, R. H. Boyer, J. L. Bolton, D. G. Burrows, D. P. Herman and M. M. Krahn. 2004. Northwest Fisheries Science Center procedures for extraction, cleanup and gas chromatography/mass spectrometry analysis of sediments and tissues for organic contaminants. NOAA Tech Memo NMFS/NWFSC-59, U. S. Department of Commerce, Seattle, WA.
62. Thomas, J. A., S. Leatherwood, W. E. Evans, J. R. Jehl and F. T. Awbrey. 1981. Ross sea killer whale distribution, behavior, color pattern and vocalizations. Antarctic Journal of the United States 1981 Review 16:157 158.
63. 13C analysis of diet. Oecologia (Berlin) 57 : 32 37.
64. Tollit, D. J., M. Steward, P. M. Thompson, G. J. Pierce, M. B. Santos and S. Hughes. 1997. Species and size differences in the digestion of otoliths and beaks: Implications for estimates of pinniped diet composition. Canadian Journal of Fisheries and Aquatic Sciences 54 : 105 119.
65. Visser, I. N. 1999. Antarctic orca in New Zealand waters? New Zealand Journal of Marine and Freshwater Research 33 : 515 520.
66. Wada, E., M. Terazaki, Y. Kabaya and T. Nemoto. 1987. N-15 and C-13 abundances in the Antarctic Ocean with emphasis on the biogeochemical structure of the food web. Deep Sea Research Part A Oceanographic Research Papers 34 : 829 841.
67. Walton, M. J., R. J. Henderson and P. P. Pomeroy. 2000. Use of blubber fatty acid profiles to distinguish dietary differences between grey seals Halichoerus grypus from two UK breeding colonies. Marine Ecology Progress Series 193 : 201 208.
68. Wania, F., and D. Mackay. 1996. Tracking the distribution of persistent organic pollutants. Environmental Science & Technology 30 : A390 A396.
69. Weber, K., and H. Goerke. 1996. Organochlorine compounds in fish off the Antarctic Peninsula. Chemosphere 33 : 377 392.
70. Weber, K., and H. Goerke. 2003. Persistent organic pollutants (POPs) in Antarctic fish: Levels, patterns, changes. Chemosphere 53 : 667 678.
71. Ylitalo, G. M., C. O. Matkin, J. Buzitis, M. M. Krahn, L. L. Jones, T. Rowles and J. E. Stein. 2001. Influence of life-history parameters on organochlorine concentrations in free-ranging killer whales (Orcinus orca) from Prince William Sound, AK. Science of the Total Environment 281 : 183 203.
72. Ylitalo, G. M., G. K. Yanagida, L. Hufnagle, Jr. and M. M. Krahn. 2005. Determination of lipid classes and lipid content in tissues of aquatic organisms using a thin layer chromatography/flame ionization detection (TLC/FID) microlipid method. Pages 449 464 in G. K. Ostrander, ed. Techniques in aquatic toxicology. CRC Press, Boca Raton, FL.
73. Yonezaki, S., M. Kiyota, N. Baba, T. Koido and A. Takemura. 2003. Size distribution of the hard remains of prey in the digestive tract of northern fur seal (Callorhinus ursinus) and related biases in diet estimation by scat analysis. Mammal Study 28 : 97 102.
74. Zhao, L. Y., M. A. Castellini, T. L. Mau and S. J. Trumble. 2004. Trophic interactions of Antarctic seals as determined by stable isotope signatures. Polar Biology 27 : 368 373.